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The long, wide, deep estuary of Milford Haven divides Pembrokeshire into two parts. The distance by road from Neyland on the north shore to Pembroke Dock on the south is 28 miles. Prior to the construction of the bridge the former County Council operated a ferry service between the two shores. This ferry was able to carry up to 24 vehicles and 250 pedestrians on each trip.

In the mid 1960's with the growth of Milford Haven as a major oil port capable of handling the world's largest tankers, it was decided to replace the vehicular ferry service with a bridge and a new road, which unlike the ferry would be available on a 24 hour basis.

Sir Alexander Gibb and Partners and Freeman Fox and Partners were appointed jointly as consulting engineers to design the Cleddau Bridge and the smaller bridge over the Westfield Pill. The new roadworks and the two bridges provided a highway link between the southern and northern towns of Pembrokeshire and between the oil refineries located along both shores of the Haven.

The contract for building the Cleddau Bridge was awarded in September 1968 to A.E. Farr Limited with Horseley Bridge and Thomas Piggott Limited as sub-contractors for the steelwork. The contract of £2.1 million was to be completed by March 1971. On 2nd June 1970 some 21 months into the contract a 60m cantilever collapsed on the south bank, tragically resulting in the loss of four lives. The construction of the bridge recommenced in 1972 with the first of the new box units to replace those damaged being erected in October 1972 some 28 months after the collapse.

The bridge was eventually opened to traffic in 1975. In the first year of operation approximately 885,900 vehicles used the bridge. By year ending March 2009 this number increased to 4,600,407 which is the highest figures recorded.